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      Preserved Crossmodal Integration of Emotional Signals in Binge Drinking

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          Abstract

          Binge drinking is an alcohol consumption pattern with various psychological and cognitive consequences. As binge drinking showed qualitatively comparable cognitive impairments to those reported in alcohol-dependence, a continuum hypothesis suggests that this habit would be a first step toward alcohol-related disorders. Besides these cognitive impairments, alcohol-dependence is also characterized by large-scale deficits in emotional processing, particularly in crossmodal contexts, and these abilities have scarcely been explored in binge drinking. Emotional decoding, most often based on multiple modalities (e.g., facial expression, prosody or gesture), yet represents a crucial ability for efficient interpersonal communication and social integration. The present study is the first exploration of crossmodal emotional processing in binge drinking, in order to test whether binge drinkers already present the emotional impairments described among alcohol-dependent patients, in line with the continuum hypothesis. Twenty binge drinkers and 20 matched controls performed an experimental task requiring the identification of two emotions (happiness or anger) presented in two modalities (visual or auditory) within three conditions (unimodal, crossmodal congruent or crossmodal incongruent). In accordance with previous research in binge drinking and alcohol-dependence, this study was based on two main hypotheses. First, binge drinkers would present a reduced facilitation effect (i.e., classically indexed in healthy populations by faster reaction times when two congruent modalities are presented simultaneously). Second, binge drinkers would have higher difficulties to inhibit interference in incongruent modalities. Results showed no significant difference between groups in emotional decoding ability, whatever the modality or condition. Control participants, however, appeared slower than binge drinkers in recognizing facial expressions, also leading to a stronger facilitation effect when the two modalities were presented simultaneously. However, findings did not show a disrupted facilitation effect in binge drinkers, whom also presented preserved performance to inhibit incongruence during emotional decoding. The current results thus suggest that binge drinkers do not demonstrate a deficit for emotional processing, both in unimodal and crossmodal contexts. These results imply that binge drinking might not be characterized by impairments for the identification of primary emotions, which could also indicate that these emotional processing abilities are well-preserved at early stages of excessive alcohol consumption.

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          Most cited references54

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          A neuromodulatory role for the human amygdala in processing emotional facial expressions.

          Localized amygdalar lesions in humans produce deficits in the recognition of fearful facial expressions. We used functional neuroimaging to test two hypotheses: (i) that the amygdala and some of its functionally connected structures mediate specific neural responses to fearful expressions; (ii) that the early visual processing of emotional faces can be influenced by amygdalar activity. Normal subjects were scanned using PET while they performed a gender discrimination task involving static grey-scale images of faces expressing varying degrees of fear or happiness. In support of the first hypothesis, enhanced activity in the left amygdala, left pulvinar, left anterior insula and bilateral anterior cingulate gyri was observed during the processing of fearful faces. Evidence consistent with the second hypothesis was obtained by a demonstration that amygdalar responses predict expression-specific neural activity in extrastriate cortex.
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            Detection of audio-visual integration sites in humans by application of electrophysiological criteria to the BOLD effect.

            Electrophysiological studies in nonhuman primates and other mammals have shown that sensory cues from different modalities that appear at the same time and in the same location can increase the firing rate of multisensory cells in the superior colliculus to a level exceeding that predicted by summing the responses to the unimodal inputs. In contrast, spatially disparate multisensory cues can induce a profound response depression. We have previously demonstrated using functional magnetic resonance imaging (fMRI) that similar indices of crossmodal facilitation and inhibition are detectable in human cortex when subjects listen to speech while viewing visually congruent and incongruent lip and mouth movements. Here, we have used fMRI to investigate whether similar BOLD signal changes are observable during the crossmodal integration of nonspeech auditory and visual stimuli, matched or mismatched solely on the basis of their temporal synchrony, and if so, whether these crossmodal effects occur in similar brain areas as those identified during the integration of audio-visual speech. Subjects were exposed to synchronous and asynchronous auditory (white noise bursts) and visual (B/W alternating checkerboard) stimuli and to each modality in isolation. Synchronous and asynchronous bimodal inputs produced superadditive BOLD response enhancement and response depression across a large network of polysensory areas. The most highly significant of these crossmodal gains and decrements were observed in the superior colliculi. Other regions exhibiting these crossmodal interactions included cortex within the superior temporal sulcus, intraparietal sulcus, insula, and several foci in the frontal lobe, including within the superior and ventromedial frontal gyri. These data demonstrate the efficacy of using an analytic approach informed by electrophysiology to identify multisensory integration sites in humans and suggest that the particular network of brain areas implicated in these crossmodal integrative processes are dependent on the nature of the correspondence between the different sensory inputs (e.g. space, time, and/or form). Copyright 2001 Academic Press.
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              Binge drinking, cognitive performance and mood in a population of young social drinkers.

              Binge drinking may lead to brain damage and have implications for the development of alcohol dependence. The aims of the present study were to determine individual characteristics as well as to compare mood states and cognitive function between binge and nonbinge drinkers and thus further validate the new tool used to identify these populations among social drinkers. The lowest and the highest 33.3% from a database of 245 social drinkers' binge scores derived from the Alcohol Use Questionnaire (AUQ) were used as cutoff points to identify nonbinge drinkers and binge drinkers in a further population of 100 young healthy volunteers. Personality characteristics, expectations of the effects of alcohol and current mood were evaluated. Cognitive performance was tested with a Matching to Sample Visual Search task (MTS) and a Spatial Working Memory task (SWM) both from the CANTAB battery, and a Vigilance task from the Gordon Diagnostic System. The binge drinkers had less positive mood than the nonbinge drinkers. In the MTS choice time on an 8-pattern condition and movement time on an 8- and 4-pattern condition was found to be faster in the binge drinkers compared to nonbinge drinkers. A gender by binge drinking interaction in the SWM and the Gordon Diagnostic System task revealed that female binge drinkers were worse on both these tasks than the female nonbinge drinkers. These results confirm previous findings in binge drinkers and suggest that in a nondependent alcohol-drinking group, differences can be seen in mood and cognitive performance between those that binge drink and those that do not.
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                Author and article information

                Contributors
                Journal
                Front Psychol
                Front Psychol
                Front. Psychol.
                Frontiers in Psychology
                Frontiers Media S.A.
                1664-1078
                15 June 2017
                2017
                : 8
                : 984
                Affiliations
                [1] 1Laboratory for Experimental Psychopathology, Psychological Science Research Institute, Université catholique de Louvain Louvain-la-Neuve, Belgium
                [2] 2Institute for Health and Behavior, Integrative Research Unit on Social and Individual Development, University of Luxembourg Esch-sur-Alzette, Luxembourg
                Author notes

                Edited by: Fernando Cadaveira, Universidade de Santiago de Compostela, Spain

                Reviewed by: Maria Teresa Cortés–Tomás, Universitat de València, Spain; Flávia L. Osório, Universidade de Ribeirão Preto, Brazil

                *Correspondence: Pierre Maurage, pierre.maurage@ 123456uclouvain.be

                This article was submitted to Psychopathology, a section of the journal Frontiers in Psychology

                Article
                10.3389/fpsyg.2017.00984
                5471335
                28663732
                d101a70c-1cb9-4e9b-ac45-be6895d40238
                Copyright © 2017 Lannoy, Dormal, Brion, Billieux and Maurage.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 04 April 2017
                : 29 May 2017
                Page count
                Figures: 2, Tables: 2, Equations: 0, References: 59, Pages: 10, Words: 0
                Funding
                Funded by: Fonds De La Recherche Scientifique - FNRS 10.13039/501100002661
                Funded by: Fondation de France 10.13039/501100004431
                Categories
                Psychology
                Original Research

                Clinical Psychology & Psychiatry
                heavy drinking,emotion,facial expression,prosody,alcohol-dependence

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